Human-Like Maternal Left-Cradling Bias in Monkeys Is Altered by Social Pressure

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OPEN Human‑like maternal left‑cradling bias in monkeys is altered by social pressure Grégoire Boulinguez‑Ambroise 1,2,3, Emmanuelle Pouydebat3, Éloïse Disarbois1 & Adrien Meguerditchian 1,2*

About 66–72% of human mothers cradle their infants on their left side. Given that left-cradling exposes the baby’s face to the mother’s left visual feld (i.e., mainly projected to her right hemisphere) and is altered by emotional states such as stress, maternal left-cradling was interpreted as refecting right-hemispheric dominance for emotional processing. Whether this phenomenon is unique to human evolution is still in debate. In the present study we followed 44 olive baboon (Papio anubis) mothers and their infants in diferent social groups. We found that a maternal cradling bias exists and is predominantly towards the left in a similar proportion as in humans, but shifts toward a right bias in mothers living in high density groups. The sensitivity of left-cradling to social pressure highlights its potential links with the mother’s stress as reported in humans. Our fnding clearly illustrates the phylogenetic continuity between humans and Old-World monkeys concerning this lateralization and its potential links with hemispheric specialization for emotions, inherited from a common ancestor 25–35 million years ago.

In Humans, about 66–72% of mothers prefer to cradle their infants on the lef side of their body midline 1. In other words, mothers hold their infant in their arms, close to their body, positioning its head in their lef peri- personal hemispace and support the weight with their lef arm2. Te lef-cradling bias persists for at least the frst 12 weeks afer birth 3. However, at the human population-level, inanimate objects (i.e., bags) are carried on the right side for the greatest part 4. However, a pillow adorned with a proto-face is enough to elicit a lef-cradling bias in children5. Tis phenomenon has raised lots of questions and studies which have shown that a contralateral relation with handedness is not present. Indeed, although lef-side maternal cradling leaves the right hand free for other activities in right-handed mothers, lef-handed individuals turn out to also present a lef-cradling bias5, (but see6,7). Besides manual preference, heart position (i.e., soothing sound of heartbeats 8–10), cultural considerations 11, or the diferent activities during which cradling occurs (i.e., rocking, nursing12–14) seem not to afect the lef-cradling bias. Te most consensual theory to date combines visual feld and cerebral hemispheric specialization. Te “right-hemisphere hypothesis” highlights the posture of a lef-cradled baby, as it exposes its face to the lef visual feld of the mother 15. Due to the contralateral organization of the human sensory systems, this visual information is mainly projected to the mother’s right brain hemisphere. As the right hemisphere of the brain is specialized in the perception of emotional facial expressions16–19, the lef-cradling bias would con- sequently favour the mother’s monitoring of the emotional state of the infant. In parallel, the lef-cradled infant looks at the lef side of the mother’s face, which has been described as being the most expressive7,20,21. It has been assessed that 3-month-old children identify the attractiveness of a face as well as adults do22. According to some authors, this direct access to the mother’s emotional state would then facilitate creating and reinforcing social bonds within the mother baby dyad15. Also, it has been shown that lef- cradling mothers judge as more attractive a lef- rather than a right-facing profle of a human baby (and vice versa for right-cradling ones)23. Recent studies 2,5 pushed the investigations on the lef-cradling bias further, showing a relationship with empathy and ill-being in humans. On the one hand, they found the strength of the lef-cradling bias to be positively related with the mother’s empathic abilities2. Moreover, children cradling a doll on their lef display higher mean social ability scores than their peers showing a right-cradling bias 5.

1Laboratoire de Psychologie Cognitive UMR7290, CNRS, Aix-Marseille Université, 3 Place Victor Hugo, 13331 Marseille Cedex 3, France. 2Station de Primatologie, CNRS, Rousset‑sur‑Arc, France. 3Mecanismes Adaptatifs et Évolution UMR 7179‑CNRS, National Museum of Natural History, 75321 Paris Cedex 5, France. *email: adrien.meguerditchian@univ‑amu.fr

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Figure 1. Maternal cradling in an adult female olive baboon. A baboon mother is cradling her baby on her lef side. Photograph copyright: Eloïse Disarbois.

On the other hand, right-side cradling is associated with higher pre-and postnatal maternal anxiety and depression24,25. Maternal depression involves decreased communication within the mother-infant dyad 26 and a dysfunction of the right brain hemisphere afecting emotional perception. It may therefore be considered as a factor that alters the lef-cradling bias 27. Other studies have found higher stress levels in mothers with a right-cradling bias, than in their counterparts cradling on the lef28. Stress can immediately impact the infant cradling: under induced physiological stress conditions (identifed by a higher blood pressure and heart rate), women hold a human-like doll more on the right 29. In both 4 and 5-year-old boys and girls, the lef-cradling bias is already strongly present when cradling a human infant-like doll, but can be reversed under unfamiliar or stressful stimuli5. Afective symptoms can therefore alter lef cradling, refecting a reduced ability to be emotion- ally involved with the infant. Facing such a biological phenomenon, a question arises: is this trait specifc to humans? Most of the work in other vertebrate species focusing on patterns of lateralization in mother-infant interactions has shown a population-level preference for keeping the mother on the lef side in infants 30. Concerning maternal cradling specifcally, which involves holding the infant close to one’s body by using the arms and hands 2, humans are not the only primate species showing this lateralized behavior, as great apes and monkeys like macaques and baboons also cradle their babies during the frst months of life. Tis behaviour is mainly female-specifc and maternal. A lef side bias in infant holding has been reported mostly in great apes 8,31,32 whereas studies in our more distant primate relatives, such as Old or New World monkeys reported no consistent cradling bias14. Te early onset of lef-cradling bias in humans and its presence in great apes suggest an evolutionary continuum of the dominance of the right brain hemisphere for processing social-emotional stimuli5,33. Te lef-cradling bias could thus be the result of biological determinism selected through natural selection rather than an intentional act. Nevertheless, no study to date has investigated the link between a lef-cradling bias and the maternal emotional state in non-human primates. In the present study we investigated (1) side-asymmetries in maternal cradling behaviours during the three frst months afer the infant’s birth in the olive baboon (Papio anubis) (see Fig. 1). We also (2) explored its potential relation with the social group density as a marker of social stress. We frst expect cradling to be lateralized in female olive baboons at the individual level and predict a population-level lef-cradling bias similar to humans. As olive baboons organize themselves into very hierarchical social groups, agonistic behaviours, social pressure and thus socially-related stress strongly increase with density34,35. If, as in humans, stress is a factor afecting the lef-cradling bias, we therefore expect the lef-cradling bias to be altered or even reversed in females housed in high densities social groups. Results Maternal cradling‑side bias at individual level. According to z-score, 40 mothers were classifed as signifcantly lateralized for maternal cradling (lef- or right-sided) while only 4 were considered as ambiguously lateralized. Out of the 18 females that had two pregnancies during the study time, the direction and strength of the individual cradling bias was very stable across infants (Pearson correlation r17 = 0.97, P < 0.0001; see Fig. 2).

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Figure 2. Plot depicting correlation between individual CBI from successive newborns. N = 18. Te maternal cradling-side bias index (CBI) is the ratio (R − L)/(R + L), where R and L respectively represent the total right and lef arm uses. It ranges from − 1 to 1. A negative ratio indicates a lef side cradling bias, whereas a positive one indicates a right-cradling bias.

In fact, 17 kept the same cradling-side bias while only one female switched from an ambiguously lateralized to a lef-biased cradling, but both cradling-side bias indices (CBI) had the same negative sign, indicating similar lef direction of the cradling-side bias. Neither an infants’ sex or maternal parity were signifcant predictors of cradling lateralization.

Maternal cradling‑side bias at population level. According to the z-score, among the 40 lateralized mothers, 27 cradled signifcantly their infant on the lef side and 13 on their right side. Tis translated into a signifcant lef-cradling bias at population-level (X2 = 4.9, P = 0.026; N = 40). Te calculation of the mean cradling- side bias index score among the total of 44 mothers, M.CBI = − 0.20, SD = 0.65, confrmed the lef-cradling bias at a population-level according to a one-sample t test (t43 = − 2.03, P = 0.047).

Efects of social group structures on the population‑level cradling‑side bias. Linear models detected that the cradling z-score signifcantly increased with increasing density (F1,42 = 5.30; P = 0.026), indicating an increase in a right cradling bias. By running a Kruskal–Wallis rank sum test with the cradling-side bias (i.e., based on z-score calculation) as a qualitative variable and the density as a quantitative variable, we found that the 27 lef cradling mothers lived in signifcant lower density social groups (mean density = 0.11) than the 13 right cradling mothers (mean density = 0.15; Kruskal–Wallis X2 = 6.14, P = 0.013; see Fig. 3A). Afer running a second linear model with the type of group structures (i.e. mono-male aviaries and parks, multi-male park) as signifcant predictor of cradling z-score (F2,41 = 4.60; P = 0.015), we made a pairwise comparison using t tests and a Bonferroni correction. When comparing females housed within mono-male groups but in high densities aviaries (t1) versus lower densities parks (t2, see Table 1), we found a strong signifcant diference (P = 0.02). Females housed in mono-male parks cradled mainly on their lef side (z-score mean = − 7.19; CBI mean = − 0.56), whereas females housed in mono-male aviaries cradled more on their right side (z-score mean = 2.36; CBI mean = 0.20). Te multi-male park (t3) showed higher variability and was not signifcantly diferent from the two other types of group structures (z-score mean = − 0.68; CI mean = − 0.08; see Fig. 3). Discussion In accordance with our predictions, we found a signifcant lef-side maternal cradling bias in an Old-World monkey, the olive baboon (Papio anubis) in an almost identical proportion (i.e. 67.45% among the 40 lateralized subjects) to the one usually found in human mothers (64% in the most recent study2). Tis fnding, which is consistent with similar evidence from great apes, namely chimpanzee (Pan troglodytes) and gorilla (Gorilla gorilla)31,32 clearly indicates that this lateralization phenomenon is not unique to humans but also present in catarrhines. Previous inconsistent results in macaques and baboons (for a review 14) are likely due (1) to too small sample sizes (i.e., from 4 to 10 subjects) preventing to draw any conclusions about population-level lateralization, or (2) to the non-consideration of the social density in a macaques’ study including a substantial sample of captive individuals 13. Interestingly, we also found that the direction and the degree of individual maternal cradling bias is consistent and stable across successive pregnancies within the same mothers. Tis suggests that, as for humans, lef-cradling bias is a robust lateralized behaviour, which might be ultimately related to the same underlying hemispheric specialization process. Te drivers of the observed convergence between olive baboons and humans remain unclear. One hypothesis is that lef-side maternal cradling might refect rightward hemispheric specialization for emotions, as has been suggested in humans 2,5,15, since it favours the mother’s lef visual feld of view (i.e. right hemisphere processing) for maternal monitoring. Given that a right hemisphere advantage for facial emotional expressions processing has been highlighted not only in humans 16, but also in other primate species, namely chimpanzees 36, rhesus monkeys 37 and baboons 38, it is not unlikely that a shared hemispheric specialization for emotion might be involved in the manifestation of the lef-cradling bias we

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Figure 3. Efect of social density on maternal cradling-side bias. (A) Boxplot of the densities of social groups housing Papio anubis females (n = 40) regarding their cradling-side bias (i.e., based on z-score and excluding 4 ambiguously lateralized cases). (B) Boxplot of the cradling z-scores of Papio anubis females according to their social group structures: high density mono-male aviaries (t1), low density mono-male parks (t2) and a high density multi-male park (t3). Adult males are in beige and females and juveniles are in purple. Te calculation of the z-score is based on the total lef and right arm uses. It provides the direction of cradling side preference: lef (< − 1.96) or right (> 1.96). (*P value < 0.05).

observed in baboons. However, this latter hypothesis needs to be tested specifcally in further investigations. In humans, lef-cradled infants look at the lef side of the mother’s face, exposing therefore their “right hemisphere” to the most expressive side of the mother’s face 7,20,21,39. Such typical lef-side cradling pattern might in turn trigger a typical neurodevelopment in the cradled infant. It has been shown that individuals who had been cradled on the mother’s right side during infancy showed a signifcant decrease of the typical lef bias for emotional faces compared to lef-cradled individuals 40. It is possible that a reduced exposure to optimal (i.e., lef) or suboptimal (i.e., right) emotional information from faces during infanthood (due to a reversed lateral holding position) might

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Habitat Aviaries (t1) Park 1 (t2) Park 2 (t2) Park 3 (t2) Park 4 (t3) Surface (m2) 28 291 291 211 267 Adult males 1 1 1 1 3 Focal mothers 11 6 6 5 16 Group size 5.57 (± 0.78) 19 21 23 38 Density 0.19(± 0.028) 0.07 0.07 0.11 0.14

Table 1. Description of the diferent habitats housing the olive baboon subjects during the study. Habitats include mono-male and multi-male social group structures. Of the 44 focal females 11 were housed in seven aviaries of same surface; the average group size and density are provided with standard deviations. Te group sizes of the four parks, where the 33 other females lived, were subject to variations as some individuals died or were moved within the station. Te table provides the maximal group sizes and densities observed in these parks during the study time.

have crucial outcomes for the ability to perceive facial emotions later in life and for cascades of other related socio-emotional abilities (thus being benefcial for the child’s later development of such functions). In this regard, based on interlocutory fndings linking the cradling-side bias with social attachment abilities41 and the presence of autistic traits 42,43, it has been very recently hypothesized that the typical/atypical holding-side during infancy might be one of the possible early signs of potential neurodevelopmental dysfunctions such as autism spectrum disorders44,45. In addition, asymmetries in an infant’s positioning have also been reported in non-primate species that do not carry their babies. In a wide range of marine and terrestrial mammals, juveniles have a strong preference for keeping their mother on their lef side, namely in their lef visual feld 30. Tis has prompted previous authors to propose the idea that the right lateralized “social brain” as described in primates has an ancient evolutionary origin. It would be derived from earlier forms of lateralization in vertebrates, namely lateralization in interactions within the mother-infant dyad that promote bonding and thus maximize the infants’ survival. Our results push the potential link between cradling and emotions further by showing that the lef-cradling bias may be an evolutive proxy of the maternal emotional state in an old-word monkey, as it is in humans2,5. More importantly, we further found lateralized cradling at the individual-level to be strongly related with demographic densities, and not group size. While mothers living in low density groups show a strong lef-cradling bias, mothers living in high density groups show a weaker lef-side bias, or even a right bias during cradling. One potential explanation of the sensitiveness in cradling bias to social density might be found in its tight relation with the mother’s social stress. According to this hypothesis, which remains to be tested, the maternal lef-cradling bias would be, just like in humans 28,29, altered by stress, which is in baboons attributed to high social density. Olive baboons organize themselves into very hierarchical social groups 46. Relationships of dominance result in a strong power struggle. Higher densities increase the occurrence and frequency of conficts involving severe aggression 34,35. Such conditions involve higher levels of stress. In humans, whereas lef-cradling bias is positively related with empathy 2 and stronger social abilities 5, it is negatively related with depression and anxiety 2,24,25. Maternal depression involves a dysfunction of the right brain hemisphere afecting the perception of emotions and may therefore alter the lef-cradling bias 27, as it is observed under stressful stimuli 28,29. Higher densities in olive baboon social groups, and thus greater social pressure, may also have a cost for the mothers by mobilizing more attentional and emotional resources in the right hemisphere to the detriment of infant’s lateralized monitoring. In fact, the several social functions, that are particularly recruited in high density groups, mobilize the right side of the brain such as (1) aggressive responses47 from dominant females ensuring their rank or, (2) processing conspecifc faces 47 in low-rank females to discern aggressive expressions, and (3) display avoidance or withdrawal behaviors47. According to this hypothesis, the socially related stress would thus alter the rightward hemispheric resources allocated to the maternal monitoring and ultimately afect the lef-cradling bias. Nevertheless, whether diferent confounding factors related to social density—other than stress—may explain this variability remains unclear. Unfortunately, no study has investigated the direct link between cradling-side bias and the maternal emotional state in non-human primate species. To test the “stress hypothesis” in non-human primates, further investigations are thus needed and should consider evaluating the potential direct links between cradling-side bias and (1) the stress level of the mother (e.g., cortisol level assessment, induced stress situation), or (2) the hemispheric specialization for emotions (e.g., brain structural correlates using in vivo MRI-imaging, behavioral asymmetry testing related to the lateralization of emotions such as facial expressions or chimeric face processing). In conclusion, we suggest that the origin of a lef-cradling bias may be much older than the origin of humans and even older than hominids and hominoids, dating back to common ancestor of humans and Old-World monkeys about 25–35 million years ago. Te convergence of fndings for baboons and humans as well as the cradling bias’s sensitiveness to social density opens the road to the hypothesis that a similar hemispheric specialization for emotion may be involved in the maternal cradling lateralization phenomenon and its alteration by stress. Methods Experimental model and subject details. All our subjects (Papio anubis) were born and raised in cap- tivity in the UPS 846 Primate Center of the C.N.R.S. (Rousset, France). We followed 44 adult mothers and 63 juveniles (from 1 day to 3 months), as 17 mothers gave birth to 2 infants and 1 mother gave birth to 3 infants successively during the time frame of the study. Olive baboons live in social groups in large aviaries or parks from 28 to 291 m2, (see Table 1). Each enclosure included an inside and an outside area. Te 44 mothers lived in

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3 diferent types of habitats and group structures (see Table 1) including (t1) mono-male multifemale structures in high density small social groups (i.e., seven aviaries); (t2) mono-male multifemale structures in low density large social groups (i.e., three parks: 1, 2, 3), and (t3) multi-male multi-female structures in large but high density social group (i.e., one park 4). Our sample of 63 infants includes 33 females and 28 males (the sex of two infants was not identifed). At the beginning of the study, 14 females were primiparous and 30 were multiparous. Eth- ics Te study was approved by the “C2EA-71 Ethical Committee of Neurosciences” (INT Marseille) under the number APAFIS#13553-201802151547729, and has been conducted at the Station de Primatologie (Rousset- Sur-Arc, France, Agreement C130877). All methods were performed in accordance with the relevant CNRS guidelines and the European Union regulations (Directive 2010/63/EU).

Procedure of data collection. Among the focal baboons’ mother-infant dyad, we quantifed the use of the lef arm versus the right arm to cradle the infant, regardless of the mother’s postures (see Fig. 1) or of feed- ing interactions. According to a behavioral sampling procedure, a minimum of 30 occurrences of cradling was collected for each dyad (min = 34, max = 784; mean = 172, SD = 151). We collected data during the three frst months afer birth, the baby being almost exclusively cradled during this period. Afer this period, mothers cradle less and less and carry the juveniles on their back or on their belly but without a support by the arm. We counted an occurrence as an independent bout of cradling. Every time the mother stopped cradling her baby— for manipulation (i.e., grooming, play) or to let him get out of the embrace—a cradling period ended; the next cradling was then reported as a new occurrence. Cradling bouts were considered only if both of the mother’s hands were free (i.e., not holding an object in one hand); thus, we assumed there was an independent choice of hands for cradling.

Statistical analysis. We frst determined the direction of cradling-side asymmetry for each mother and each infant by calculating a z-score, based on the total lef and right arm uses48. We then classifed each mother as having a lef side (z ≤ − 1.96) or right side (z ≥ 1.96) cradling bias, or behaving ambiguously (− 1.96 < z < 1.96). We also quantifed the degree of the cradling-side bias for each subject by calculating an individual cradling-side bias index score (CBI) using the formula (R − L)/(R + L). R and L respectively represent the total right and lef arm uses48,49. A negative value indicates a lef side cradling bias, whereas a positive value a right-side bias. We performed the following statistical analyses: (1) we performed a Pearson correlation test to assess whether direction and strength of the individual cradling bias were stable across ofspring or not. We selected the females who had 2 pregnancies successively within our study period, and correlated the mother’s CBI for the frst infant with the one for the second infant. (2) We additionally ran a multiple linear regression to test efects of experi- ence (i.e., parity), and infant’s sex as predictors of cradling lateralization (i.e., z-score). (3) We tested for a lef- cradling bias at a population level by performing a Chi-squared test for given probabilities (0.5, 0.5) comparing the number of mothers cradling their infant on the lef side versus on their right side (classifcation based on z-scores). (4) We also tested for a population-level lef-cradling bias by calculating the mean cradling-side bias index score, and running a one-sample t test. (5) In order to test an efect of social density on the population-level lef-cradling bias, we ran a linear model with density as quantitative predictor of cradling z-score. We further ran (6) a Kruskal–Wallis rank sum test with the cradling-side bias (i.e., based on z-score calculation) as a qualitative variable and the density as a quantitative variable. (7) Afer running a second linear model with the type of group structures (i.e. mono-male aviaries and parks, multi-male park) as signifcant predictor of cradling z-score, we made a pairwise comparison using t tests and the Bonferroni P value adjustment method. We checked normality by performing a Shapiro–Wilk Normality test. We used the following RStudio packages: FactoMineR, car, MASS, readxl. All statistics were performed using a conventional level of signifcance (P = 0.05). Data availability Te datasets supporting this article have been uploaded as part of the supplementary material. Tey will be moved to an external repository upon publication.

Received: 30 April 2020; Accepted: 17 June 2020

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We warmly thank Pascaline Boitelle (veterinarian) and the animal keepers of the CNRS UPS 846. Te project has received funding from the European Research Council under the European Union’s Horizon 2020 research and innovation program Grant Agreement No. 716931—GESTIMAGE—ERC-2016-STG (P.I. Adrien

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Meguerditchian), as well as from the French “Agence Nationale de la Recherche” (ANR-16-CONV-0002 (ILCB), ANR-11-LABX-0036 (BLRI) and ANR-11- 656 IDEX-0001-02 (A*MIDEX)). Author contributions G.B.A, E.P., and A.M. designed the experiment. A.M. supervised the study. G.B.A. and E.D. conducted the experiments. G.B.A ran the statistical analyses. G.B.A. wrote the frst draf. G.B.A. and A.M. fnalized the draf in addressing also comments of E.P., E.D. and of two anonymous reviewers. All authors gave fnal approval for publication and agree to be held accountable for the work performed therein.

Competing interests Te authors declare no competing interests. Additional information Supplementary information is available for this paper at https://doi.org/10.1038/s41598-020-68020-3. Correspondence and requests for materials should be addressed to A.M. Reprints and permissions information is available at www.nature.com/reprints. Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional afliations. Open Access Tis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Te images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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